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Vibrio Species in an Urban Tropical Estuary: Antimicrobial Susceptibility, Interaction with Environmental Parameters, and Possible Public Health Outcomes

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Vibrio Species in an Urban Tropical Estuary: Antimicrobial Susceptibility, Interaction with Environmental Parameters, and Possible Public Health Outcomes microorganisms Article Vibrio Species in an Urban Tropical Estuary: Antimicrobial Susceptibility, Interaction with Environmental Parameters, and Possible Public Health Outcomes Anna L. B. Canellas 1 , Isabelle R. Lopes 1 , Marianne P. Mello 2, Rodolfo Paranhos 2, Bruno F. R. de Oliveira 1 and Marinella S. Laport 1,* 1 Laboratório de Bacteriologia Molecular e Marinha, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941902, Brazil; [email protected] (A.L.B.C.); [email protected] (I.R.L.); [email protected] (B.F.R.d.O.) 2 Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro 21941617, Brazil; [email protected] (M.P.M.); [email protected] (R.P.) * Correspondence: [email protected] Abstract: The genus Vibrio comprises pathogens ubiquitous to marine environments. This study evaluated the cultivable Vibrio community in the Guanabara Bay (GB), a recreational, yet heavily polluted estuary in Rio de Janeiro, Brazil. Over one year, 66 water samples from three locations along a pollution gradient were investigated. Isolates were identified by MALDI-TOF mass spectrometry, revealing 20 Vibrio species, including several potential pathogens. Antimicrobial susceptibility testing confirmed resistance to aminoglycosides, beta-lactams (including carbapenems and third-generation cephalosporins), fluoroquinolones, sulfonamides, and tetracyclines. Four strains were producers Citation: Canellas, A.L.B.; Lopes, of extended-spectrum beta-lactamases (ESBL), all of which carried beta-lactam and heavy metal I.R.; Mello, M.P.; Paranhos, R.; de resistance genes. The toxR gene was detected in all V. parahaemolyticus strains, although none carried Oliveira, B.F.R.; Laport, M.S. Vibrio tdh trh Species in an Urban Tropical Estuary: the or genes. Higher bacterial isolation rates occurred in months marked by higher water Antimicrobial Susceptibility, temperatures, lower salinities, and lower phosphorus and nitrogen concentrations. The presence Interaction with Environmental of non-susceptible Vibrio spp. was related to indicators of eutrophication and sewage inflow. DNA Parameters, and Possible Public fingerprinting analyses revealed that V. harveyi and V. parahaemolyticus strains non-susceptible to Health Outcomes. Microorganisms antimicrobials might persist in these waters throughout the year. Our findings indicate the presence 2021, 9, 1007. https://doi.org/ of antimicrobial-resistant and potentially pathogenic Vibrio spp. in a recreational environment, raising 10.3390/microorganisms9051007 concerns about the possible risks of human exposure to these waters. Academic Editor: Danny Morick Keywords: antimicrobial resistance; Guanabara Bay; marine pollution; public health; Vibrio Received: 13 April 2021 Accepted: 3 May 2021 Published: 7 May 2021 1. Introduction Vibrio Publisher’s Note: MDPI stays neutral The genus includes Gram-negative curved rod-shaped Gammaproteobacteria with regard to jurisdictional claims in autochthonous in aquatic environments, where they play important roles in nutrient published maps and institutional affil- cycling [1]. These bacteria comprise a remarkably diverse group and are known not only iations. for their ability to rapidly adapt to environmental changes but also for their intrinsic competency to acquire and transmit exogenous DNA via horizontal gene transfer (HGT) events, especially among pathogenic strains [2]. Vibrio spp. can be found either in a free-living state or associated with marine animals and particles, such as plastics and phytoplankton [1,3]. Currently, there are 123 validated species according to the Genome Copyright: © 2021 by the authors. Vibrio cholerae Vibrio vulnificus Vibrio parahaemolyticus Licensee MDPI, Basel, Switzerland. Taxonomy Database [4]. From these, , , , This article is an open access article and Vibrio alginolyticus are the four species, also known as the “big four”, often associated distributed under the terms and with human infections [5]. conditions of the Creative Commons Vibrio spp. infections usually occur via the consumption of contaminated seafood or Attribution (CC BY) license (https:// exposure to contaminated water and tend to be self-limiting. However, they can be fatal, creativecommons.org/licenses/by/ especially in immunocompromised patients or upon failure of antimicrobial therapy [6,7]. 4.0/). Although cholera cases are mostly reported in areas where water quality is inadequate and Microorganisms 2021, 9, 1007. https://doi.org/10.3390/microorganisms9051007 https://www.mdpi.com/journal/microorganisms Microorganisms 2021, 9, 1007 2 of 18 sewage treatment insufficient, other Vibrio species are relevant agents of seafood-borne infections on a global scale. In fact, the genus Vibrio along with 13 other pathogens are accountable for more than 95% of foodborne infections and subsequent hospitalizations in the United States and responsible for 98% of deaths [8]. Moreover, extraintestinal infections caused by Vibrio spp., such as ear and wound infections, have been gaining more attention in view of the consequences of climate change, which have been linked to a rise in such cases [5,9]. There is currently an absence of surveillance systems dedicated to Vibrio illnesses outside the United States, a country where these data have been gathered since 1989 through “The Cholera and Other Vibrio Illness Surveillance” (COVIS) system [10]. Hence, there may be an underestimation of Vibrio spp. infections worldwide. Albeit usually susceptible to most of the currently used antibacterial drugs, resistant Vibrio spp. have been reported with increasing frequency in many countries over the past years, raising concerns about the remaining treatment options and food safety [11,12]. Although widely investigated under the clinical framework, there is a significant knowledge gap regarding the antimicrobial resistance issue in environmental settings, notably aquatic ecosystems. The presence of clinically relevant traits in environmental bacteria, such as certain antimicrobial and heavy metal resistance genes, poses a challenge to public health and supports the hypothesis that anthropogenic action is one of the most important evolutionary forces on the planet [13]. Since aquatic environments often serve as recreational areas and sources of subsistence to the population, it is fundamental to better understand the risks they may pose to human health, in particular their active role as hotspots of virulent and/or antimicrobial-resistant microorganisms [14]. Potentially pathogenic Vibrio spp. have been previously isolated in the Guanabara Bay (GB), Rio de Janeiro, Brazil [15,16]. However, little attention has been paid to the investigation of their antimicrobial susceptibility and monitoring of their spatio-temporal dynamics in this ecosystem. The GB is a eutrophic estuarine system located in a humid tropical region surrounded by the second major metropolitan area in Brazil. GB is the second-largest bay on the Brazilian coast with a surface area of approximately 384 km2 and a volume of 1.87 × 109 m3 [17]. In its surroundings, there are more than 15 cities, thousands of industries, refineries, two ports, and several shipyards. In addition, circa 10 million people live in GB’s surroundings, from which around 4 million live in informal settlements with precarious sanitary and urbanization conditions. On account of the lack of proper sewage collection and treatment, the GB is chronically impacted by untreated sewage (~18 m3/s), petroleum residues, littering, and the discharge of industrial, rural, and hospital effluents [18,19]. Despite the fact that the GB receives water from the Atlantic Ocean and several rivers and streams, its inner regions are often considered inappropriate for bathing according to local monitoring services [20]. Nonetheless, navigation, fishing, and swimming are common activities in the area. The GB shares some characteristics with other impacted environments in the world, such as the Bay of Bengal, known to be vulnerable to water-borne diseases and pollu- tion [21]. In 2018, local monitoring systems in Rio de Janeiro’s metropolitan area have reported more than 1200 hospitalizations and more than 30 deaths on account of water- borne illnesses [22]. Also, many studies worldwide indicate that individuals who are directly in contact with recreational waters, e.g., swimming or fishing, are more likely to develop certain illnesses, such as gastrointestinal infections [23,24]. Despite being a major aquatic ecosystem in this region, little is known about the risks of exposure to GB’s waters to human health. Therefore, this study aimed to investigate the cultivable Vibrio community in three distinct locations along a pollution gradient in the GB over a one-year period (2018–2019). By doing so, we observed that potentially pathogenic Vibrio strains are present in GB’s waters and that they can be resistant to multiple antimicrobials. DNA fingerprinting analyses further indicated that groups of resistant strains belonging to the same species are present in the GB throughout the year. Moreover, the most ecologically impacted location presented not only the highest bacterial abundance but also the highest rates of antimicrobial-resistant bacteria harboring beta-lactam and heavy metal resistance Microorganisms 2021, 9, 1007 3 of 18 genes. Correlation analyses suggest that Vibrio abundance is linked with eutrophication and sewage inflow indicators. The occurrence of
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